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Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis

Rago, Alfredo LU ; Werren, John H. and Colbourne, John K. (2020) In PLoS Genetics 16(1).
Abstract

Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks... (More)

Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks show sex-biased functional interactions in early developmental stages. These networks provide new candidates for hymenopteran sex determination, including histone modification. In contrast, sex-bias in pupae and adults is driven by the differential expression of genes. We observe sex-biased isoform switching consistently across development, but mostly in genes that are already differentially expressed. Finally, we discover that sex-biased networks are enriched by genes specific to the Nasonia clade, and that those genes possess the topological properties of key regulators. These findings suggest that regulators in sex-biased networks evolve more rapidly than regulators of other developmental networks.

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author
; and
publishing date
type
Contribution to journal
publication status
published
in
PLoS Genetics
volume
16
issue
1
article number
e1008518
publisher
Public Library of Science (PLoS)
external identifiers
  • scopus:85079090323
  • pmid:31986136
ISSN
1553-7390
DOI
10.1371/journal.pgen.1008518
language
English
LU publication?
no
additional info
Funding Information: The research was supported by US National Institutes of Health grant to JHW (1R24GM084917 ?Genetic and Genomic Tools for the Emerging Model Organism, Nasonia?) including a sub-award to JKC. Additional support was provided to JKC by the University of Birmingham, and to JHW by the US National Science Foundation (IOS-1456233) and Nathaniel & Helen Wisch Chair. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publisher Copyright: © 2020 Rago et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
id
2f487399-9936-4834-a22f-055e46387d54
date added to LUP
2022-01-26 12:14:37
date last changed
2024-06-01 23:49:18
@article{2f487399-9936-4834-a22f-055e46387d54,
  abstract     = {{<p>Sexual dimorphism requires regulation of gene expression in developing organisms. These developmental differences are caused by differential expression of genes and isoforms. The effect of expressing a gene is also influenced by which other genes are simultaneously expressed (functional interactions). However, few studies have described how these processes change across development. We compare the dynamics of differential expression, isoform switching and functional interactions in the sexual development of the model parasitoid wasp Nasonia vitripennis, a system that permits genome wide analysis of sex bias from early embryos to adults. We find relatively little sex-bias in embryos and larvae at the gene level, but several sub-networks show sex-biased functional interactions in early developmental stages. These networks provide new candidates for hymenopteran sex determination, including histone modification. In contrast, sex-bias in pupae and adults is driven by the differential expression of genes. We observe sex-biased isoform switching consistently across development, but mostly in genes that are already differentially expressed. Finally, we discover that sex-biased networks are enriched by genes specific to the Nasonia clade, and that those genes possess the topological properties of key regulators. These findings suggest that regulators in sex-biased networks evolve more rapidly than regulators of other developmental networks.</p>}},
  author       = {{Rago, Alfredo and Werren, John H. and Colbourne, John K.}},
  issn         = {{1553-7390}},
  language     = {{eng}},
  number       = {{1}},
  publisher    = {{Public Library of Science (PLoS)}},
  series       = {{PLoS Genetics}},
  title        = {{Sex biased expression and co-expression networks in development, using the hymenopteran Nasonia vitripennis}},
  url          = {{http://dx.doi.org/10.1371/journal.pgen.1008518}},
  doi          = {{10.1371/journal.pgen.1008518}},
  volume       = {{16}},
  year         = {{2020}},
}